Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin
Open accessAbstract
BACKGROUND: Preeclampsia has been considered an anti-angiogenic state. Two factors have been implicated in the genesis of this state: soluble vascular endothelial growth factor receptor-1 (sVEGFR-1) and placental growth factor (PlGF). Indeed, the concentrations of PlGF, an angiogenic factor, are lower in preeclampsia than in normal pregnancy, while the opposite is the case for the anti-angiogenic factor, sVEGFR-1. The source of the excess sVEGFR-1 has not yet been determined. Since the placenta could be a source of sVEGFR-1, we conducted a study to determine whether there is a gradient in the plasma concentration of sVEGFR-1 and PlGF between the uterine vein and the antecubital vein in both patients with preeclampsia and normal pregnant women. METHODS: A cross-sectional study was performed to determine the plasma concentrations of sVEGFR-1 and PlGF in the uterine and antecubital vein of patients with preeclampsia (n = 9) and normal pregnant women at term (n = 9). Plasma samples were collected from antecubital and uterine veins at the time of cesarean section. The concentrations of sVEGFR-1 and PlGF were determined using specific enzyme-linked immunoassays. The differences of plasma concentrations of sVEGFR-1 and PlGF between uterine and antecubital veins in both groups were compared by paired t-tests. RESULTS: Patients with preeclampsia had a significantly higher mean plasma concentration of sVEGFR-1 in the uterine vein than in the antecubital vein (uterine vein: mean 13,675 +/- 5,684 pg/ml vs. antecubital vein: mean 10,234 +/- 4,700 pg/ml; paired t-tests, p = 0.04). In contrast, among normal pregnant women at term, there was no significant difference in plasma concentrations of sVEGFR-1 between the uterine and antecubital veins (uterine vein: mean 1,918 +/- 665 pg/ml vs. antecubital vein: mean 1,750 +/- 475 pg/ml; paired t-tests, p = 0.1). The mean plasma concentration of sVEGFR-1, either in the antecubital or uterine vein, was significantly higher in preeclampsia than in normal pregnancy (unpaired t-tests; both p < 0.001). There was no significant difference in the mean plasma concentration of PlGF between the uterine and the antecubital veins in both the preeclamptic (uterine vein, mean +/- SD: 129 +/- 106 pg/ml vs. antecubital vein, mean +/- SD: 82 +/- 43 pg/ml; paired t-tests, p = 0.2) and normal pregnancy groups (uterine vein, mean +/- SD: 331 +/- 254 pg/ml vs. antecubital vein, mean +/- SD: 319 +/- 259 pg/ml; paired t-tests, p = 0.4). The mean plasma concentration of PlGF, either in the uterine or antecubital vein, was lower in preeclampsia than in normal pregnancy (unpaired t-tests; p = 0.008 and 0.02 respectively). CONCLUSIONS: Plasma concentration of sVEGFR-1 was higher in the uterine vein than in the antecubital vein in women with preeclampsia. This provides evidence supporting the concept that the uterus is a potential source of the excess circulating sVEGFR-1 concentration in preeclamptic women.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
There is excessive production of sVEGFR-1 and soluble endoglin in the uterus of preeclamptic patients proportional to the severity of the disease.
“There is excessive production of sVEGFR-1 and soluble endoglin in the uterus of preeclamptic patients(121) proportional to the severity of the disease (151–153)”
From Metformin, the Aspirin of the 21st Century: Its Role in Gestational Diabetes Mellitus, Prevention of Preeclampsia and Cancer, and the Promotion of Longevity (2017) · cites this paper as [121]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The biology of VEGF and its receptors
Ferrara, N., Gerber, H.-P., & LeCouter, J. (2003) · Nature Medicine · doi:10.1038/nm0603-669 · Cited by 9,591 · see citing works
Maynard, S. E., Min, J.-Y., Merchan, J., Lim, K.-H., Li, J., Mondal, S., Libermann, T. A., Morgan, J. P., Sellke, F. W., Stillman, I. E., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17189 · Cited by 4,101 · see citing works
A united states national reference for fetal growth
Alexander, G. M., Himes, J. H., Kaufman, R. H., Mor, J. M., & Kogan, M. D. (1996) · Obstetrics and Gynecology · doi:10.1016/0029-7844(95)00386-x · Cited by 2,294 · see citing works
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Gerber, H. P., McMurtrey, A. E., Kowalski, J., Yan, M., Keyt, B. A., Dixit, V. M., & Ferrara, N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.46.30336 · Cited by 1,976 · see citing works
Preeclampsia: an endothelial cell disorder
Roberts, J. M., Taylor, R. N., Musci, T. J., Rodgers, G. M., Hubel, C. A., & McLaughlin, M. K. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90665-0 · Cited by 1,859 · see citing works
Preeclampsia: An excessive maternal inflammatory response to pregnancy
Redman, C. W. G., Sacks, G. P., & Sargent, I. L. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70239-5 · Cited by 1,838 · see citing works
A Study of Angiotensin II Pressor Response throughout Primigravid Pregnancy
Gant, N. F., Daley, G. L., Chand, S., Whalley, P. J., & MacDonald, P. C. (1973) · Journal of Clinical Investigation · doi:10.1172/jci107462 · Cited by 1,218 · see citing works
Kaufmann, P., Black, S., & Huppertz, B. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.014977 · Cited by 1,210 · see citing works
Diagnosis and Management of Gestational Hypertension and Preeclampsia
Sibai, B. M. (2003) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(03)00475-7 · Cited by 1,149 · see citing works
Sacks, G. P., Studená, K., Sargent, I. L., & Redman, C. W. G. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70254-6 · Cited by 823 · see citing works
Etiology and pathogenesis of preeclampsia: Current concepts
Dekker, G., & Sibai, B. M. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70160-7 · Cited by 760 · see citing works
Zhou, Y., McMaster, M., Woo, K., Janatpour, M. J., Perry, J., Kärpänen, T., Alitalo, K. K., Damsky, C. H., & Fisher, S. J. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62567-9 · Cited by 639 · see citing works
Development of the placental villous tree and its consequences for fetal growth
Kingdom, J. C., Huppertz, B., Seaward, G. R., & Kaufmann, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00423-1 · Cited by 591 · see citing works
Ishihara, N., Matsuo, H., Murakoshi, H., Laoag‐Fernandez, J. B., Samoto, T., & Maruo, T. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.119176 · Cited by 509 · see citing works
Placental Debris, Oxidative Stress and Pre-eclampsia
Redman, C. W. G., & Sargent, I. L. (2000) · Placenta · doi:10.1053/plac.2000.0560 · Cited by 508 · see citing works
Knight, M., Redman, C., Linton, E. A., & Sargent, I. L. (1998) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1998.tb10178.x · Cited by 496 · see citing works
He, H., Venema, V. J., Gu, X., Venema, R. C., Marrero, M. B., & Caldwell, R. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.35.25130 · Cited by 488 · see citing works
Risk factors associated with preeclampsia in healthy nulliparous women
Sibai, B. M., Ewell, M., Levine, R. J., Klebanoff, M. A., Esterlitz, J., Catalano, P. M., Goldenberg, R. L., & Joffe, G. M. (1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70004-8 · Cited by 483 · see citing works
Placental Cytokines and the Pathogenesis of Preeclampsia
Conrad, K. P., & Benyo, D. F. (1997) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1997.tb00222.x · Cited by 479 · see citing works
Tsatsaris, V., Goffin, F., Munaut, C., Brichant, J.-F., Pignon, M.-R., Noël, A., Schaaps, J., CABROL, D., Frankenne, F., & Foidart, J. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030528 · Cited by 461 · see citing works
Clark, D. E., Smith, S. K., He, Y., Day, K. A., Licence, D. R., Corps, A. N., Lammoglia, R., & Jones, D. S. (1998) · Biology of Reproduction · doi:10.1095/biolreprod59.6.1540 · Cited by 413 · see citing works
Koga, K., Osuga, Y., Yoshino, O., Hirota, Y., Ruimeng, X., Hirata, T., Takeda, S., Yano, T., Tsutsumi, O., & Taketani, Y. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021942 · Cited by 403 · see citing works
Chaiworapongsa, T., Romero, R., Espinoza, J., Bujold, E., Mee Kim, Y., Gonçalves, L. F., Gomez, R., & Edwin, S. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.03.043 · Cited by 368 · see citing works
Self-citationChaiworapongsa, T., Romero, R., Kim, Y. M., Kim, G. J., Kim, M. R., Espinoza, J., Bujold, E., Gonçalves, L., Gomez, R., Edwin, S., et al. (2005) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050400028816 · Cited by 359 · see citing works
Self-citationDiFederico, E., Genbacev, O., & Fisher, S. J. (1999) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)65123-1 · Cited by 348 · see citing works
Pathophysiology of Preeclampsia: Linking Placental Ischemia/Hypoxia with Microvascular Dysfunction
Granger, J. P., Alexander, B. T., Llinás, M. T., Bennett, W. A., & Khalil, R. A. (2002) · Microcirculation · doi:10.1038/sj.mn.7800137 · Cited by 334 · see citing works
Expression of Inflammatory Cytokines in Placentas from Women with Preeclampsia1
Benyo, D. F., Smárason, A. K., Redman, C. W. G., Sims, C. J., & Conrad, K. P. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7585 · Cited by 329 · see citing works
Shore, V. H., Wang, T.-H., Wang, C. L., Torry, R. J., Caudle, M. R., & Torry, D. S. (1997) · Placenta · doi:10.1016/s0143-4004(97)90007-2 · Cited by 325 · see citing works
Clark, D. E., Smith, S. K., Sharkey, A., et al. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019303 · Cited by 288 · see citing works
Huppertz, B., Kingdom, J. C., Caniggia, I., Desoyé, G., Black, S., Korr, H., & Kaufmann, P. (2003) · Placenta · doi:10.1053/plac.2002.0903 · Cited by 288 · see citing works
Increased placental apoptosis in pregnancies complicated by preeclampsia
Leung, D. N., Smith, S. C., To, K. F., Sahota, D. S., & Baker, P. N. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.112906 · Cited by 281 · see citing works
Role of Placenta in Preeclampsia
Myatt, L. (2002) · Endocrine · doi:10.1385/endo:19:1:103 · Cited by 272 · see citing works
Horowitz, J. R., Rivard, A., van der Zee, R., Hariawala, M. D., Sheriff, D. D., Esakof, D. D., Chaudhry, G. M., Symes, J. F., & Isner, J. M. (1997) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.17.11.2793 · Cited by 266 · see citing works
Morphological Changes in the Utero-Placental Bed in Pregnancy Hypertension
Brosens, I. A. (1977) · Clinics in Obstetrics and Gynaecology · doi:10.1016/s0306-3356(21)00411-8 · Cited by 247 · see citing works
Trophoblast Deportation in Human Pregnancy—its Relevance for Pre-eclampsia
Johansen, M., Redman, C. W. G., WILKINS, T., & Sargent, I. L. (1999) · Placenta · doi:10.1053/plac.1999.0422 · Cited by 223 · see citing works
Huppertz, B., Frank, H., Reister, F., Kingdom, J. C., Korr, H., & Kaufmann, P. (1999) · PubMed · Cited by 209 · see citing works
A clinical test useful for predicting the development of acute hypertension in pregnancy
Gant, N. F., Chand, S., Worley, R. J., et al. (1974) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(74)90170-7 · Cited by 205 · see citing works
Renin-angiotensin system in normal and toxemic pregnancies
Talledo, O. E., Chesley, L. C., & Zuspan, F. P. (1968) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)33724-8 · Cited by 204 · see citing works
Khaliq, A., Dunk, C., Jiang, J., et al. (1999) · PubMed · Cited by 194 · see citing works
Trophoblast deportation in pre‐eclamptic pregnancy
Chua, S., WILKINS, T., SARGENT, I. L., & Redman, C. W. G. (1991) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1991.tb15334.x · Cited by 188 · see citing works
Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia
Gervasi, M.-T., Chaiworapongsa, T., Pacora, P., Naccasha, N., Yoon, B. H., Maymon, E., & Romero, R. J. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.117311 · Cited by 182 · see citing works
Self-citationCockell, A., Learmont, J. G., Smárason, A. K., Redman, C. W. G., Sargent, I. L., & Poston, L. (1997) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1997.tb11052.x · Cited by 171 · see citing works
The pathogenesis of pre-eclampsia
Redman, C. W. G., & Sargent, I. L. (2001) · Gynécologie Obstétrique & Fertilité · doi:10.1016/s1297-9589(01)00180-1 · Cited by 169 · see citing works
Activation of Leukocytes During the Uteroplacental Passage in Preeclampsia
Mellembakken, J. R., Aukrust, P., Olafsen, M. K., Ueland, T., Hestdal, K., & Videm, V. (2002) · Hypertension · doi:10.1161/hy0102.100778 · Cited by 169 · see citing works
Clark, B. A., Halvorson, L. M., Sachs, B. P., et al. (1992) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(92)91372-h · Cited by 155 · see citing works
Ahmed, A., Dunk, C., Kniss, D. A., & Wilkes, M. (1997) · PubMed · Cited by 153 · see citing works
Zhou, Y., Bellingard, V., Feng, K.-T., McMaster, M., & Fisher, S. J. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00449-4 · Cited by 143 · see citing works
Athanassiades, A., & Lala, P. K. (1998) · Placenta · doi:10.1016/s0143-4004(98)91039-6 · Cited by 142 · see citing works
Kumazaki, K., Nakayama, M., Suehara, N., & Wada, Y. (2002) · Human Pathology · doi:10.1053/hupa.2002.129420 · Cited by 141 · see citing works
Angiogenesis and intrauterine growth restriction
Ahmed, A., & Perkins, J. (2000) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1053/beog.2000.0139 · Cited by 134 · see citing works
Circulating Factors as Markers and Mediators of Endothelial Cell Dysfunction in Preeclampsia
Taylor, R. N., de Groot, C. J. M., Cho, Y., & Lim, K.-H. (1998) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016249 · Cited by 133 · see citing works
Athanassiades, A., Hamilton, G. S., & Lala, P. K. (1998) · Biology of Reproduction · doi:10.1095/biolreprod59.3.643 · Cited by 128 · see citing works
The nature of pressor responsiveness to angiotensin II in human pregnancy.
Gant, N. F., Chand, S., Whalley, P. J., & MacDonald, P. C. (1974) · PubMed · Cited by 126 · see citing works
Expression and Function of Placenta Growth Factor: Implications for Abnormal Placentation
Torry, D., Mukherjea, D., Arroyo, J. A., & Torry, R. J. (2003) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(03)00048-0 · Cited by 102 · see citing works
Gliki, G., ABU-GHAZALEH, R., Jezequel, S., Wheeler-Jones, C. P. D., & Zachary, I. C. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3530503 · Cited by 99 · see citing works
Invasive cytotrophoblast apoptosis in pre-eclampsia
Genbačev, O., DiFederico, E. M., McMaster, M., & Fisher, S. J. (1999) · Human Reproduction · doi:10.1093/humrep/14.suppl_2.59 · Cited by 98 · see citing works
Toxemia: new concepts in an old disease.
Romero, R. J., Lockwood, C. J., Enrique Oyarzún, E., et al. (1988) · PubMed · Cited by 94 · see citing works
Self-citationPlacental vascular morphogenesis
Jones, D. S., & Burton, G. J. (2000) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1053/beog.2000.0137 · Cited by 93 · see citing works
Nitric oxide in the uteroplacental, fetoplacental, and peripheral circulations in preeclampsia
Norris, L. (1999) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(99)00007-1 · Cited by 89 · see citing works
McKinney, E. T., Shouri, R., Hunt, R., et al. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.108877 · Cited by 86 · see citing works
Signal Transduction and Biological Function of Placenta Growth Factor in Primary Human Trophoblast1
Desai, J., Holt, V. J., Torry, R. J., Caudle, M. R., & Torry, D. S. (1999) · Biology of Reproduction · doi:10.1095/biolreprod60.4.887 · Cited by 86 · see citing works
The Effects of Angiogenic Growth Factors on Extravillous Trophoblast Invasion and Motility
Lash, G. E., Cartwright, J. E., Whitley, G., et al. (1999) · Placenta · doi:10.1053/plac.1999.0427 · Cited by 81 · see citing works
Higgins, J. R., Walshe, J. J., Darling, M., Norris, L., & Bonnar, J. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70389-8 · Cited by 75 · see citing works
Angiogenesis and placental growth in normal and compromised pregnancies
Ong, S. S., Lash, G. E., & Baker, P. N. (2000) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1053/beog.2000.0138 · Cited by 75 · see citing works
A pressor substance (hysterotonin) occurring in toxemia
Hunter, C. A., & Howard, W. F. (1960) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(60)90676-1 · Cited by 66 · see citing works
Neale, D. M., Demasio, K. A., Illuzzi, J. L., Chaiworapongsa, T., Romero, R. J., & Mor, G. (2003) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/jmf.13.1.39.44 · Cited by 60 · see citing works
Self-citationDefinitive Molecular Evidence of Renin-Angiotensin System in Human Uterine Decidual Cells
Li, C., Ansari, R. A., Yu, Z., et al. (2000) · Hypertension · doi:10.1161/01.hyp.36.2.159 · Cited by 60 · see citing works
Placenta Growth Factor: Potential Role in Pregnancy
Torry, D. S., Ahn, H., Barnes, E. L., & Torry, R. J. (1999) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1999.tb00078.x · Cited by 59 · see citing works
Gliki, G., ABU-GHAZALEH, R., Jezequel, S., et al. (2001) · Biochemical Journal · doi:10.1042/bj3530503 · Cited by 58 · see citing works
Higgins, J. R., Papayianni, A., Brady, H. R., Darling, M., & Walshe, J. J. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70380-1 · Cited by 57 · see citing works
von Dadelszen, P. (1999) · Human Reproduction · doi:10.1093/humrep/14.4.919 · Cited by 56 · see citing works
Plasma glutathion S-transferase-Alpha levels in preeclampsia and HELLP syndrome
Steegers, E. A. P., Mulders, T. M. T., Penders, R. H. M. J., et al. (1996) · Radboud Repository (Radboud University) · Cited by 50 · see citing works
Lash, G. E., Taylor, C. M., Trew, A. J., et al. (2003) · Growth Factors · doi:10.1080/0897719021000069560 · Cited by 50 · see citing works
Catecholamines. Their role in pregnancy and the development of pregnancy-induced hypertension.
Zuspan, F. P. (1979) · PubMed · Cited by 45 · see citing works
Pathophysiology of Preeclampsia: Linking Placental Ischemia/Hypoxia with Microvascular Dysfunction
Granger, J. P., Alexander, B. T., Llinás, M. T., et al. (2002) · Microcirculation · doi:10.1080/mic.9.3.147.160 · Cited by 44 · see citing works
Perinatal implications of maternal hypertension
Shah, D. M. (2001) · Seminars in Pediatric Neurology · doi:10.1053/spen.2001.25812 · Cited by 30 · see citing works
A proposed relationship between vasopressinase altered vasopressin and preeclampsia
Krege, J. H., & Katz, V. L. (1990) · Medical Hypotheses · doi:10.1016/0306-9877(90)90020-f · Cited by 23 · see citing works
The hypertensive action of blood from patients with pre-eclampsia
Tatum, H. J., & Mulé, J. G. (1962) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(16)35936-1 · Cited by 22 · see citing works
The effect of plasma retransfusion on the blood pressure in the puerperium
Pirani, B. B. K., & MacGillivaray, I. (1975) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(75)90644-4 · Cited by 19 · see citing works
Pedersen, E. B., Aalkjær, C., CHRISTENSEN, N. J., et al. (1984) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365518409085377 · Cited by 12 · see citing works
Elmer, D. B., Granai, C. O., Ball, H. G., et al. (1993) · PubMed · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 8
- Romero R. Prenatal medicine: The child is the father of the man. Prenat Neonat Med 1996;1:8-11.
- Roberts JM. Pregnancy related hypertension. In: Creasy RK, Resnik R (editors). Maternal fetal medicine. Philadelphia: WB Saunders; 1998. pp 883-892.
- Huppertz B, Kadrov M, Black S, et al. Maternal anemia and preeclampsia display opposite invasive phenotype and reduced apoptosis of interstitial extravillous trophoblast. J Soc Gynecol Investig 2003;10:316A.
- Williams J. Premature seperation of the normally implanted placenta. Surg Gynecol Obstet 1915;21:541-554.
- Charnock-Jones DS, Burton GJ. Placental vascular morpho- genesis. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:953-968.
- Schlembach D, Beinder E. Angiogenic factors in preeclamp- sia. J Soc Gynecol Investig 2003;10:316A.
- Page EW, Cox AJ. Renal chnages following toxaemias of late pregnancy. West J Surg 1983;46:463.
- Tatum HJ, Mule JG. The hypertensive action of blood from preeclampsia. Am J Obstet Gynecol 1962;83:1028-1034.
Cited by
Sorted by citations
Pre-eclampsia part 1: current understanding of its pathophysiology
Chaiworapongsa, T., Chaemsaithong, P., Yeo, L., & Romero, R. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.102 · Cited by 956 · see citing works
Self-citationRomero, R., Erez, O., Hüttemann, M., Maymon, E., Panaitescu, B., Conde-Agudelo, A., Pacora, P., Yoon, B. H., & Grossman, L. I. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.06.003 · Cited by 253 · see citing works
Self-citationSzalai, G., Romero, R., Chaiworapongsa, T., Xu, Y., Wang, B., Ahn, H., Xu, Z., Chiang, P. J., Sundell, B., Wang, R., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119547 · Cited by 46 · see citing works
Self-citationHolme, A. M., Roland, M. C. P., Henriksen, T., & Michelsen, T. M. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.07.056 · Cited by 45 · see citing works
Oggè, G., Romero, R., Kusanovic, J. P., Chaiworapongsa, T., Dong, Z., Mittal, P., Vaisbuch, E., Mazaki-Tovi, S., Gonzalez, J. M., Yeo, L., et al. (2010) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767050903366119 · Cited by 25 · see citing works
Self-citation
- Authors
- Bujold, E., Romero, R., Chaiworapongsa, T., KIM, Y. M., Kim, G. J., Kim, M. R., Espinoza, J., Gonçalves, L. F., Edwin, S., & Mazor, M.
- Affiliations
- Wayne State University (US)
- United States Department of Health and Human Services (US)
- Perinatology Research Branch, NICHD/NIH/DHHS, Bethesda, Maryland
- Department of Obstetrics and Gynecology, Wayne State University/Hutzel Women's Hospital, Detroit, Michigan
- Ben-Gurion University of the Negev (IL)
- Corresponding author
- Bujold, Emmanuel
- ORCID
- Venue
- The Journal of Maternal-Fetal & Neonatal Medicine
- Publisher
- Informa UK Limited
- Published
- 2005-07
- Volume
- 18
- Issue
- 1
- Pages
- 9-16
- ISSN
- 1476-4954 (ISSN-L)
- 1476-7058
- OpenAlex
- W2028131307
- Cited by
- 110
- References
- 82
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 8 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 8 · 2017: 6 · 2016: 7 · 2015: 8 · 2014: 6 · 2013: 8 · 2012: 5
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Maternal-Fetal & Neonatal Medicine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Psychiatry and Mental health › Neurological Complications and Syndromes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- preeclampsia, soluble fms-like tyrosine kinase-1, placental growth factor, uterine vein, antecubital vein, maternal plasma, angiogenic factors, placenta, cesarean section, term pregnancy, placental insufficiency, placental hypoxia
- MeSH terms
- Placenta Growth Factor, Adult, Cross-Sectional Studies, Elbow, Female, Humans, Placenta, Pre-Eclampsia, Pregnancy, Pregnancy Proteins, Uterus, Vascular Endothelial Growth Factor Receptor-1
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
